Multiple origins of a sex ratio supergene in Formica ants

Abstract

Many known supergenes, regions of the genome containing two or more functional mutations with little or no recombination between them, formed in recent evolutionary time to control complex traits. However, when supergenes persist through millions of years of evolution, they may take on additional functions in different lineages. Here, we investigate how an ancient supergene has evolved to gain novel function. In Formica ants, most species have an ancient "social" supergene with M and P haplotypes which determine whether a colony is headed by a single queen or multiple queens, respectively. At least three Formica species have an additional haplotype on the same chromosome, termed MD, associated with female-biased offspring sex ratio at the colony level. Is an MD haplotype present in additional species? Do the MD haplotypes share a common origin or did they evolve convergently? With whole-genome resequencing, we identify MD haplotypes in three additional species and use variation across six Formica species to examine the evolutionary history of the MD haplotype. We find that the MD haplotype did not originate from a rearrangement of the ancestral M haplotype. Instead, the MD haplotype likely originated from recombination between the M and P haplotypes. Strikingly, we identified two putative origins of the MD haplotype, one in the ancestor of five Nearctic species, and a second in the Palearctic species F. cinerea. The discovery of two MD haplotypes convergently evolving from distinct recombination events between two ancestral supergene haplotypes illustrates how supergenes can diversify and gain additional phenotypes.